Journal Journal of Entomological of Entomological and andAcarological Acarological Research Research 2017; 2012; volume volume 49:6679 44:e

SHORT PAPER First evidence of Halyomorpha halys (Stål) ( , ) feeding on rice (Oryza sativa L.)

D. Lupi,1 P. Dioli,2 L. Limonta1 1Department of Food, Environmental and Nutritional Sciences, University of Milan; 2Museo Civico di Storia Naturale di Milano, Milan,

et al., 2014). The invasion of other regions by BMSB began in the Abstract mid-1990s in the USA when H. halys was recorded in Pennsylvania and after few years it had spread to 40 states The brown marmorated stink bug, Halyomorpha halys (Stål) is (Hoebeke & Carter, 2003). This species is now established in the a pest of numerous annual and perennial crops. Additional distribu- United States of America (Northeastern IPM Center, 2014), in tion records for H. halys are provided from northern Italy where rice Canada and in Central and Southern America (Haye et al., 2015). is cultivated, and the presence of adults feeding on panicles gives In , it was first recorded from in 2007 the first evidence of an association between this pest and rice (Oryza (Wermelinger et al., 2008).only In Italy it has been reported from var- sativa L.), a crop not previously recorded as a host plant. ious different regions since 2012 (Maistrello et al., 2013; 2014; Cesari et al., 2015; Limonta et al., 2016). It is continuing to extend its distribution in Switzerland, , , , Hungary, Liechtenstein,use , , Serbia (Haye et al., Introduction 2015), Russia (Mityushev, 2016) and Spain (Dioli et al., 2016). H. halys has also been intercepted twice in Britain (Malumphy, Halyomorpha halys (Stål) (Hemiptera Heteroptera, 2014). As with other invasive pentatomids (Dioli & Grazioli, Pentatomidae), commonly known as the brown marmorated stink 2012), BMSB can rapidly spread to new areas through human bug (BMSB), is native to East Asia (China, Korea, and Japan) (Xu transportation and the movement of goods, particularly agricultur- al commodities. The rapid spread of BMSB in Italy has also been facilitated by the climate, which provides excellent conditions for the survival and establishment of large populations of the pest Correspondence: Daniela Lupi, Department of Food, Environmental and Nutritional Sciences (DeFENS), University of Milano, via Celoria (Zhu et al., 2012). 2, 20133 Milano, Italy. H. halys, like most pentatomids, has a broad host range that E-mail: [email protected] allows it to feed and survive in fruit orchards and legume crops. Lee et al. (2013a) report more than 100 host plants in 45 families from Key words: Brown marmorated stink bug; BMSB; rice; grain; damages; 45 Asian publications. Due to its great host flexibility, H. halys has new host. rapidly become a key pest of many annual and perennial crops in invaded countries (Lee, 2015). In the United States, the has Acknowledgements: the authors thank Roberto Scherini for the photo, the rice farmer Riccardo BraggioNon-commercial for observational records, and caused economic losses valued at 21 billion dollars due to direct National Rice Research Institute rice production statistics. commodity damage, market loss, management costs, and rejection of exports (USDA-NIFA SCRI, 2013; Leskey et al., 2012). In Italy, Contributions: the authors contributed equally. economic damages has been observed close to harvest in peach and pear orchards and also in apricots, plums, apples, persimmons, and Conflict of interest: the authors declare no potential conflict of interest. tomatoes (Pansa et al., 2013; Bariselli et al., 2016). Feeding injury by H. halys results in seed loss, punctures, fruit Received for publication: 2 March 2017. Revision received: 10 April 2017. deformation, suberization, formation of spongy areas, fruit abor- Accepted for publication: 10 April 2017. tion, necrosis, and also destroyed pods (Lee, 2015). Adults and nymphs are extremely active and can readily move between differ- ©Copyright D. Lupi et al., 2017 ent cultivated and ornamental host plants (Lee et al., 2013b). Licensee PAGEPress, Italy Recently BMSB was detected in many of the rice areas in the Journal of Entomological and Acarological Research 2017; 49:6679 Po plain in Italy, but due to its polyphagy its role in the crop doi:10.4081/jear.2017.x6679 remained uncertain. As a consequence, its status in rice needs to This article is distributed under the terms of the Creative Commons be further evaluated, despite the fact that BMSB is widely distrib- Attribution Noncommercial License (by-nc 4.0) which permits any uted in other rice-producing countries and rice has not been iden- noncommercial use, distribution, and reproduction in any medium, tified as a host plant in the published literature. Rice production in provided the original author(s) and source are credited. Europe has been threatened by the exotic rice water weevil Lissorhoptrus oryzophilus Kuschel (Coleoptera: Curculionidae)

[Journal of Entomological and Acarological Research 2017; 49:6679] [page 67] Short paper which has compromised production in this economically important crop and rice paddies are interspersed with populated areas. Due to crop (Lupi et al., 2009; 2013a; 2013b), and consequently concern the distinctive characteristics of the different instars of the insect has arisen about the possible association of H. halys with rice. (Hoebeke & Carter, 2003), visual observations were made directly Several species of Pentatomidae are known to attack rice and to in paddy fields and in nearby areas from late August to the end of cause economic losses in many rice-producing countries (Table 1). October 2016. Damage is caused by adults and nymphs feeding on kernels in milk Observations are discussed comparing previous records of and dough stage of maturation, resulting in partially or totally BMSB (author’s communication, published records and the internet). unfilled grains (Lee et al., 1993; Pathak & Khan, 1994; Patel et al., 2006, Kiritani, 2007). Trophic activity can also open an access to fungi and bacteria that are responsible for pecky rice, which leads to chalky discoloration around the feeding site (Hollay et al., 1987; Results and discussion Panizzi et al., 2000). This study provides the first direct observations of BMSB Earlier records exist of Halyomorpha halys from different rice feeding on cultivated rice crops. areas in Northern Italy and also from Milan and Pavia provinces, however the insect was has not previously been directly associated with rice crops. Even though rice is cultivated in 129 Piedmont and 216 Lombardy Municipalities (data courtesy of Italian National Rice Materials and Methods Research Institute, 2016), only 14 records of this species have pre- viously been reported from the rice area, mainly in 2016 (Table 2). The research was carried out in the rice growing areas of the The observations carried out in rice crops in the Lombardy Po Valley in the Lombardy region of Italy. The two main rice pro- Region resulted in two records of BMSB on rice in Pavia Province: ducing provinces (Milan and Pavia) are contiguous, and they are the first detection of the species on panicles was on the 24th characterized by a fragmented landscape in which rice is the main September 2016 in Linaroloonly (45°9’47”88 N 09°16’15”60 E) and a

Table 1. List of the major species of Hemiptera Pentatomidae associated to rice according to geographic distribution. Distribution Species use Literature North America Oebalus pugnax (F.) Naresh & Smith, 1984; Foster et al., 1989; Espino et al., 2008 Scotinophara coarctata (F.) Heinrichs et al., 1987 Nezara viridula L. Viator et al., 1993 Central America (Cuba) Oebalus ornatus (Sailer) Pantoja et al., 1993 South America Oebalus peoecilus (Dallas) Albuquerque, 1993; Pathak & Khan,1994 Oebalus ypsilon-griseus (De Geer) Pathak & Khan,1994 Oebalus grisescens (Sailer) Pathak & Khan,1994 Tantia antiguensis (Westwood) Litsinger et al. 1986 Tantia perditor (Fabricius) Litsinger et al. 1986 Tibraca limbativentris Stal. Alves et al., 2016 Europe Aelia rostrata Boheman Süss et al., 2008 pudicus (Pd.) Süss et al., 2008 Eurigaster Laporte Süss et al., 2008 Nezara viridula L. Süss et al., 2008 Asia Dolycoris indicus Stal. Litsinger et al. 1986 Eysarcoris ventralis (Westwood) Litsinger et al. 1986 PygomenidaNon-commercial varipennis (Westwood) Pathak & Khan,1994 Pygomenida bengalensis (Westwood) Pathak & Khan,1994 Scotinophara scotti Hovarth Litsinger et al. 1986 Nezara viridula L. Pathak & Khan, 1994 Asia (Southeast) Scotinophara coarctata (F.) Barrion et al., 1982 Scotinophara cinerea (Le Guillou) Mochida, 1988 Scotinophara latiuscola Bredding Mochida, 1988 Scotinophara lurida (Burmeister) Mochida, 1988 Scotinophara. serrata (Vollenhoven) Mochida, 1988 Asia (Philippines) Scotinopara tarsalis (Vollenhoven) Litsinger et al., 1986 Asia (Japan) Lagynotomus elongatus (Dallas) Takeuchi et al., 2004 Africa Aspavia armigera F. Ewete & Olagbaju, 1990 Macrina iuvenca Burmeister Litsinger et al., 1986 Nezara viridula L. Pathak & Khan,1994 Tantia gelii Schout Litsinger et al., 1986 Australia Anaxilaus vesiculosus (Herrich-Schaeffer) Stevens et al. 2008 Eysarcoris trimaculatus (Distant) Stevens et al. 2008 Nezara viridula (L.) Stevens et al. 2008

[page 68] [Journal of Entomological and Acarological Research 2017; 49:6679] Short paper second record was obtained a month later on 20th October 2016, in Zeme (45°11’74 N;8°38’25 E) nearly 60 km away. The probing References activity on rice grain shown in Figure 1 provides evidence that the insect is attracted to rice for feeding. ALBUQUERQUE G.S., 1993 - Planting time as a tactic to manage Whilst the presence of H. halys in the Piedmont and Lombardy the small rice stink bug, Oebalus poecilus (Hemiptera, rice areas has been well documented, the nature and extent of the Pentatomidae), in Rio Grande do Sul, Brazil. - Crop Prot. 12 feeding damage that could be inflicted to rice by BMSB requires (8): 627-630. further investigation. The majority of municipalities in which H. ALVES T.M., MAIA A.H., BARRIGOSSI J.A., 2016 - Spatial dis- halys has been detected so far are, have only low levels of rice pro- tribution and coexisting patterns of adults and nymphs of duction. The findings from 2014 in Novara and in 2016 in Pavia, Tibraca limbativentris (Hemiptera: Pentatomidae) in paddy the major rice areas in Piedmont and in Lombardy respectively, rice fields. - Env. Ent. 45 (6): 1505-1514. demonstrates that the insect is still spreading in the rice area and BARISELLI M., BUGIANI R., MAISTRELLO L., 2016 - highlights the need for further work on the association between Distribution and damage caused by Halyomorpha halys in BMSB and rice. Italy. - EPPO Bull. 46 (2): 332-334. As rice cultivars differ in susceptibility to invasive species BARRION A.T., JOSHI R.C., SEBASTIAN L.S., 2008 - attack (Lupi et al., 2009; 2013b) and also to the development of Occurrence and distribution of the invasive rice black bugs pecky rice in response to pentatomid feeding (Lorenz & Hardke, Scotinophara spp. (Hemiptera: Pentatomidae) in the 2013), particular attention should be paid to the association of H. Philippines. - International Rice Research Institute. Available halys with specific cultivars and to the level of damage inflicted. from: www.scribd.com/.../occurence-and-distributionof-the- The timing of feeding relative to the developmental stage of the invasive-rice-black bug. crop should be assessed, as the amount and the type of rice stink BARRION A.T., MOCHIDA O., LITSINGER J.A., DELA CRUZ bug damage depends upon the stage of rice kernel development. N., 1982 - The Malayan black bug Scotinophara coarctata (F.) (Hemiptera: Pentatomidae): a new rice pest in the Philippines. - Int. Rice Res. New. 7 (6): 6-7. CESARI M., MAISTRELLOonly L., GANZERLI F., DIOLI P., REBECCHI L., GUIDETTI R., 2015 - A pest alien invasion in progress: potential pathways of origin of the brown marmorat- ed stink bug Halyomorpha halys populations in Italy. - J. Pest Sc. 88 (1): 1-7. COLDIRETTI,use 2016 - Assalto della cimice asiatica nel Mantovano, pere a rischio. - Available fromhttp://www.itali- afruit.net/DettaglioNews/35868/mercati-e-imprese/assalto- della-cimice-asiatica-nel-mantovano-pere-a-rischio [Accessed 24.02.2017] DIOLI P., GRAZIOLI L., 2012 - Prime segnalazioni di Lygaeus creticus Lucas, 1854 per il Veneto e altre regioni dell’Italia peninsulare (Insecta, Heteroptera, Lygaeidae). - Boll. Museo St. Nat. Venezia 63:19-25. DIOLI P., LEO P., MAISTRELLO L., 2016 - Primera cita para España y Cerdeña de la especie invasora Halyomorpha halys (Stål, 1855), con apuntes sobre su distribución en Europa (Hemiptera, Figure 1. Adult of Halyomorpha halys feeding on rice grain in the Pentatomidae). - Rev. Gadit. Entomol. 7 (1): 539-548. field (photo Roberto Scherini). ESPINO L., WAY M.O., WILSON L.T., 2008 - Determination of Oebalus pugnax (Hemiptera: Pentatomidae) spatial pattern in Non-commercial

Table 2. Municipality in Piedmont and Lombardy rice areas where Halyomorpha halys (Stål) was detected. Region Municipalities (Province) Rice area, Ha Geographic coordinates Sources Piedmont Savigliano (Cuneo) 28.88 44°3853 N - 7°39 24 E Pansa et al., 2013 Casale Monferrato (Alessandria) 1777.21 45°08′00″ N - 8°27′09″ E Pansa et al., 2013 S.Giuliano Nuovo (Alessandria) 88.42 44°54′33″ N - 8°36′36″ E Forum Ent. Ital., 2015 Roasio (Vercelli) 13.99 45°36′16″ N - 8°17′05″ E Forum Nat. Med., 2016 Novara 4387.97 45°26′48″ N - 8°37′16″ E Forum Nat. Med., 2014 Lombardy Settimo Milanese (Milano) 6 45°28’10”N ′ ″ - 9°42’64”′ ″E Forum Nat. Med.,.2013 San Donato Milanese (Milano) 36 45°2338 N - 9°17 27 E Forum Nat. Med., 2013 Rice Park (Milano) 650 45°27′55″ N - 9°11′11″ E Forum Nat. Med., 2015 Lodi 91.82 45°18′35″ N - 9°30′03″ E Coldiretti 2016 San Martino Siccomario (Pavia) 481 45°09′48″ N - 9°08′26″ E Authors record 2016 Pavia 1318.35 45°11'7"44′ ″ N - 9°9'45"′ ″ E La provincia pavese 2016 Voghera (Pavia) 22.46 44°5929 N - 9°00 42 E Voghera news 2016 Mantova 6.27 45°09′37″ N - 10°47′ 52″ E Gazzetta di Mantova 2016 Ostiglia (Mantova) 80.27 45°04′11″ N - 11°08′05″ E Gazzetta di Mantova 2016 ′ ″ ′ ″ [Journal of Entomological and Acarological Research 2017; 49:6679] [page 69] Short paper

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